Mouth breathing reduces oral function in adolescence

Although humans breathe naturally through the nostrils, mouth breathing in children has recently gathered attention. In this study, we hypothesized that tongue function and its related maxillofacial morphology would affect breathing in adolescence. To verify this hypothesis, we examined the association between breathing patterns, including mouth and nasal breathing; oral functions, including tongue motor function; and craniofacial morphology during adolescence, which has not been investigated till date. C3-H, which indicates the anteroposterior position of the hyoid bone in relation to the third cervical vertebra, was significantly smaller in mouth-breathers than in nasal-breathers. Lip-closing force, tongue pressure, and masticatory efficiency were lower in the order of nasal-breathers, oronasal-breathers, and mouth-breathers, and the values for mouth-breathers were significantly lower than those for nasal-breathers. Tongue pressure alone was identified as a significant independent variable, with an odds ratio of 1.063 (95% confidence interval, 1.006–1.123; p < 0.05). Our results indicate a relationship between mouth breathing and the lip-closing force, tongue pressure, and masticatory efficiency, as well as the significance of tongue pressure on mouth breathing in adolescents. The findings highlight the importance of clarifying the pathophysiology of mouth breathing and its underlying causes.

to the lip-closing force, tongue motor function plays an important role in sucking in infancy and mastication in later life.Mastication, in which various oral organs, including the lips and tongue, cooperate with each other, is considered closely related to mouth breathing.However, this association has not yet been fully investigated.Regarding the correlation between mouth breathing and masticatory efficiency, Sugawara et al. 22 and Sakaguchi 23 reported a significant prolongation of chewing time and a decrease in masticatory efficiency during acute nasal obstruction.However, these studies compared the effects of artificial nasal obstruction using nose clips with those of normal conditions in adults.Thus, little information is available on children with habitual mouth breathing.
In order to figure out what triggers mouth breathing as the ultimate goal of research project, we hypothesized that the factors that cause delayed development and inadequate acquisition of oral functions, especially tongue movement functions, may be related to factors that lead to mouth breathing.We believed that during the growth process from infancy to early childhood, various environmental factors such as food and childcare prevent sufficient activity of the tongue and surrounding muscles during sucking and mastication.Mouth breathing subsequently develops due to the lack of coordination between the tongue, lip, and mandibular movements.Its continuation leads to the establishment of mouth-breathing through the skeletal development of the lower face, which is disadvantageous to nasal breathing, during school-age and adolescence.This hypothesis is based on Moss's functional-matrix theory 24 , which states that the functional development of muscles and soft tissues greatly influences bone formation.As mentioned above, tongue function plays an important role from sucking in infancy to chewing and swallowing later in childhood.However, oral functions including tongue function, maxillofacial morphology, and their relationship in mouth-breathers have not been clarified.
In this study, we hypothesized that tongue function and its related maxillofacial morphology would affect breathing in adolescence to figure out the cause of oral breathing as the ultimate goal of our research project.To verify this hypothesis, we examined the association between breathing patterns, including mouth and nasal breathing; oral functions, including tongue motor function; and craniofacial morphology during adolescence, which has not been investigated till date.
Table 3 presents the craniofacial morphometry results.The SNA and SNB angles were smaller in mouthbreathers than in nasal-breathers; that is, the upper and lower jaws tended to be retracted.However, the differences were not statistically significant.ANB angle was not also statistically significant in each breathing group.The FMA and ANS-Me values were larger in the order of nasal-breathers, oronasal-breathers, and mouthbreathers, which were the so-called "high-angle cases".These values were significantly higher in mouth-breathers than in nasal-breathers.MP-H, which indicates the vertical position of the hyoid bone relative to the mandible, was larger in mouth-breathers than in nasal-breathers.This suggests a lower position of the hyoid bone relative to the mandible; however, the difference was not statistically significant.C3-H, which indicates the anteroposterior position of the hyoid bone in relation to the third cervical vertebra, was significantly smaller in mouth-breathers than in nasal-breathers.This suggests that the hyoid bone in mouth-breathers was significantly closer to the cervical vertebra and posterior to the cranium compared to that in nasal-breathers.PNS-P, which indicates the length of the soft palate, was significantly smaller in mouth-breathers than in nasal-breathers.In consideration of the sex differences, the results were compared by standardizing with a mean value of 0 and standard deviation  Table 4 shows the mean and standard deviation of oral-function values for each breathing group.For all measurements, the values for mouth-breathers were lower than those for nasal-breathers.Particularly, lip-closing force, tongue pressure, and masticatory efficiency were lower in the order of nasal-breathers, oronasal-breathers, and mouth-breathers, and the values for mouth-breathers were significantly lower than those for nasal-breathers.
Table 5 presents the results of the binomial logistic regression analysis after adjusting for age.The variance inflation factors for the maximum occlusal force and occlusal contact area were 9.96 and 10.17, respectively, and the maximum occlusal force was selected because it was a functional parameter.Tongue pressure alone was identified as a significant independent variable, with an odds ratio of 1.063 (95% confidence interval, 1.006-1.123;p < 0.05).The goodness of fit of the model was confirmed using the χ2 and Hosmer-Lemeshow tests, and percentage of correct classification (Model χ2 test, p < 0.05; Hosmer-Lemeshow test, 0.067; percentage of correct classification, 66.7%).

Discussion
Of the 103 participants included in this study, 21 (20.4%) were mouth-breathers.The prevalence of mouthbreathers has been reported in several previous studies; Humphrey et al. studied 1033 infants aged 2-5 years, of whom 220 (21%) were mouth-breathers 25 .In a study of children aged 4-6 years, Kogue et al. reported a prevalence of 22.8% 26 , whereas Shindo reported a prevalence of 29.0% in a survey of elementary-school students 27 .Thus, most studies on the proportion of mouth-breathers have focused on young children, and studies on adolescents (age > 13 years) are lacking.As mouth breathing has been gathering attention not only in medicine and dentistry but also in various other fields, the present study's identification of mouth breathing among adolescents is noteworthy.The prevalence of mouth-breathers in this study was similar to that reported in previous studies on infants and elementary school children, suggesting that mouth breathing may have appeared at an early age.
Regarding the association between mouth breathing and malocclusion, previous studies have reported a higher prevalence of malocclusion in mouth-breathers than in nasal-breathers 28,29 .Although this tendency was www.nature.com/scientificreports/observed in our study, the association was not statistically significant.Genetic factors have been considered to markedly influence the morphology of the dentition and occlusion; however, functional factors, such as breathing and habits, have also been reported as contributors 30 .Previous studies have reported a significant association between maxillary protrusion and mouth breathing 31,32 .Evaluation of the craniofacial morphology revealed that in mouth-breathers, the inclination of the mandibular plane to the Frankfort plane and lower-face height were greater and the mandible was rotated posteriorly compared to those in nasal-breathers.These results are consistent with those of previous studies [33][34][35] .Regarding MP-H, which is an index of the vertical position of the hyoid bone, no significant difference was observed between nasal and mouth-breathers.Previous studies have reported that the hyoid bone of children with mouth breathing is positioned higher in relation to the mandible and cervical vertebrae compared to that in children with nasal breathing [36][37][38] ; however, the hyoid bone in mouth-breathers was lower than that in nasal-breathers when the head was extended 39,40 , therefore, a consensus on this is lacking.Juliano et al. reported that the hyoid bone descends with age and that MP-H was not significantly different between mouth-and nasal-breathing children, but a significant difference was identified in adults 41 .Considering that this study included adolescents aged 12-25 years, age may have influenced the results.Regarding C3-H, which indicates the anteroposterior positional relationship of the hyoid bone, in this study, the hyoid bone was located closer to the cervical vertebrae and more posterior to the cranium in mouth-breathers than in nasal-breathers.In a study targeting participants aged 6-12 years, Chung et al. reported that mouth-breathers presented smaller C3-H values than nasal-breathers 37 ; other studies have also reported similar results 38,42 .In this study, PNS-P, which indicates the length of the soft palate, was significantly smaller in mouth-breathers than in nasal-breathers.Although several previous studies have reported a relationship between PNS-P and obstructive sleep apnea syndrome 43,44 , the differences between mouth and nasal-breathers have not yet been investigated.Obstructive sleep apnea syndrome is characterized by sleep-disordered breathing due to a large PNS-P.In this study, PNS-P was smaller in mouth-breathers, possibly because the soft palate extends with age, and the mean age of mouth-breathers in this study (15.6 ± 1.8 years) was lower than that of nasal-breathers (16.7 ± 3.0 years).A more detailed study of this aspect, including anatomical structures, is warranted.
Regarding oral function, the lip-closing force, tongue pressure, and masticatory efficiency were significantly lower in the mouth-breathing group than in the nasal-breathing group.Saitoh et al. reported that incompetent lips are representative of the physical appearance of mouth breathers 45 , with several similar reports showing a significant association between the two.A shift in the breathing pattern from nasal to mouth breathing causes buccal tension, lip laxity, tongue hypotonia, and decreased muscle activity in the posterior neck and anterior temporal muscles [46][47][48] .In this study, mouth-breathers presented a decrease in oral functions compared to nasalbreathers.Because the measurement of oral function is a self-administered test, the reliability of the measured values is low in younger patients.In this study, a decline in oral function was observed in mouth-breathers during adolescence, which is the earliest age when self-administered tests are possible.
The present study revealed that adolescent mouth-breathers have a posteriorly positioned hyoid bone, a posteriorly rotated mandible, and decreased oral functions, such as lip-closing force, tongue pressure, and masticatory efficiency, compared to nasal-breathers.The occurrence of these maxillofacial morphological and functional phenomena in adolescent mouth-breathers indicate that issues in early childhood may influence the condition, considering that the percentage of mouth-breathers in adolescence was not different from that in early childhood, and that no significant relationship was found between mouth breathing and malocclusion in adolescence.Furthermore, although several studies have reported an association between mouth breathing and lip-closing force, in this study, logistic regression analysis revealed a significant effect of tongue pressure on mouth breathing among adolescents.Haishima et al. reported the significance of tongue movements during infancy: infants are natural nasal-breathers who effectively perform sucking movements by fixing the hyoid bone in the anterosuperior position and suppressing the mouth-opening function of the function of the suprahyoid muscle group to open the mandible, thereby stabilizing the mandible and enabling rapid wave-like movements of the tongue 49 .Therefore, the tongue plays a vital role during early infancy.However, concern exists regarding the inadequate development of sucking movements or tongue muscles because of an inappropriate eating environment and childcare posture from infancy to early childhood.To clarify the triggers of mouth breathing as the ultimate goal of this research project, we hypothesized that the living environment may decrease the strength of the muscles surrounding the hyoid bone, causing dysfunction in the posterior positioning of this bone, disruption of the tongue's contact with the soft palate, backward rotation of the mandible, mouth breathing, jaw closing muscle inhibition 50 , and reduction in the lip-closing force, all of which are interrelated.We believe that our results, including the results of the logistic regression analysis, support our research hypothesis focused on the correlation between mouth breathing and tongue function, which had not been examined till date.Although this was a cross-sectional study in adolescents, it was the first step to assess our hypothesis that tongue problems in infancy affect the acquisition of maxillofacial morphology and oral function in adolescence.Future cross-sectional studies with a wider age range, including infancy and early childhood, as well as long-term longitudinal studies are required.The present study included 21 mouth-breathers and 57 nasal-breathers, and post-hoc analysis was performed using a free software (G*power 3.1.9.7, Heinrich-Heine-University, Düsseldorf, Germany).The results showed that α = 0.05, the effect size derived from the mean and standard deviation was 0.73, and the power was 0.81, suggesting that the sample size of this study was acceptable.However, the effect of bias on the number of participants cannot be ruled out because the sampling in this study was based on participants attending a single dental clinic.Therefore, in future, the population size should be increased to eliminate this effect considering stratification by age.Breathing patterns were assessed using a questionnaire for comparison with previous data.Quantitative evaluation methods for mouth breathing include measuring the amount of nitric oxide secreted from the sinus mucosa and separately evaluating the air in nasal and mouth-breathers; however, both methods require the use of a mask, hindering the measurement in a more physiological and natural condition in children.Understanding and responding to breathing patterns has become increasingly important in various fields, including medicine and dentistry, and the development of a more objective and simpler quantitative evaluation method for mouth breathing is expected.

Conclusion
In adolescence, compared to nasal-breathers, mouth-breathers have morphological differences (a more posteriorly positioned hyoid bone and posteriorly rotated mandible) and significantly lower oral functions (such as lipclosing force, tongue pressure, and masticatory efficiency), with tongue pressure significantly influencing mouth breathing.Our results indicate a relationship between mouth breathing and the lip-closing force, tongue pressure, and masticatory efficiency, as well as the significance of tongue pressure on mouth breathing in adolescents.The findings highlight the importance of clarifying the pathophysiology of mouth breathing and its underlying causes.

Breathing pattern
Breathing patterns were assessed using a questionnaire consisting of two questions based on the report by Kogue et al. 26 , as follows: (1) Do you often open your mouth during the day, and (2) Do you sometimes sleep with your mouth open?Those who answered "yes" to both questions were classified as "mouth-breathers, " those who answered "no" to both questions were classified as "nasal-breathers, " and the remaining were classified as "oronasal-breathers." We first interviewed the examinees themselves, and if they answered "I don't know," we interviewed their parents or guardians to obtain their opinions.

Malocclusion
The presence of reversed occlusion, open bite, maxillary protrusion, overbite, crossbite, and crowding was assessed by analyzing plaster casts according to the Japanese Association of School Dentists' criteria 51 .All the assessments were performed by a single pedodontist (Y.M.).

Oral function
The maximum occlusal force, occlusal-contact area, lip-closing force, tongue pressure, and masticatory efficiency were assessed to evaluate oral function.The maximum occlusal force and occlusal-contact area were measured using Dental Prescale II (GC, Tokyo, Japan) with the participants seated such that the head was not fixed to the headrest, and the Frankfurt plane was parallel to the floor.Participants were instructed to bite the Prescale sheet for 3 s, and the maximum occlusal force was measured using a bite-force analyzer (GC, Tokyo, Japan).Lip-closing force was measured using Lippule-kun® (Shofu, Kyoto, Japan).An oral screen-like appliance connected to the device was placed in the oral vestibule.During the measurements, participants sat with the Frankfort plane parallel to the floor.They were instructed beforehand regarding the following measurement conditions: resisting traction using the muscle strength of the lips alone, not resisting traction using a sucking force, and not bending the head and body forward while resisting.The maximum force applied to pull the oral screen-like appliance horizontally was measured as the lip-closing force.
Tongue pressure was measured using a tongue pressure-measuring instrument (JMS Co., Hiroshima, Japan).A disposable balloon probe was inserted into the participants' mouth, and participants were instructed to hold the probe gently with their front teeth and press their tongue against the pressure-sensing portion of the probe with maximum force for 7 s.The maximum pressure on the balloon was recorded as the tongue pressure, and the mean of three measurements was used as the representative value.
Masticatory efficiency was assessed using a masticatory ability testing system (Gluco Sensor GS-II; GC Co., Tokyo, Japan).The participants were asked to chew 2 g of gummy jelly for 20 s on their habitual chewing side and then gently expectorate it with 10 mL of water.The glucose level in the eluted filtrate, which was measured using the abovementioned device, reflected the masticatory efficiency.

Craniofacial morphology
The craniofacial morphology was assessed using a lateral cephalogram (Veraviewepocs 3DF X550 100CP; Morita, Osaka, Japan).Participants were instructed to stand with the Frankfurt plane parallel to the floor.Ear rods were inserted into the bilateral external auditory canals, and the head was fixed.The radiograph was obtained after the participants were asked to swallow and bite in the intercuspal position.A dentist (T.G.) trained in cephalometric https://doi.org/10.1038/s41598-024-54328-x

Table 1 .
Percentage of patients presenting each breathing-pattern.

Table 2 .
Prevalence of malocclusion in each breathing-pattern group.

Table 5 .
Results of the binomial logistic regression analysis after adjusting for age.*P < 0.05; SE, standard error.CI, confidence interval.Model x 2 test P < 0.05; Hosmer-Lemeshow test = 0.067; Percentage of correct classification = 66.7%.Vol:.(1234567890)Scientific Reports | (2024) 14:3810 | https://doi.org/10.1038/s41598-024-54328-x A total of 103 patients (49 males and 54 females; age, 12-25 years [mean, 16.6 ± 2.7 years]) who underwent regular checkups at a general dental clinic since childhood and visited the clinic between March 2021 and April 2022 after the onset of second molar eruption were included in this study.Patients undergoing orthodontic treatment and those who have completed orthodontic treatment were also excluded.This study was approved by the Ethics Review Committee of the Tokushima University Hospital for Life Science and Medical Research (Approval No., 3912) and was conducted in accordance with the Declaration of Helsinki.Informed consent was obtained from all participants or their guardians.Mothers and children completed an interview sheet regarding basic attributes such as sex, age, and lifestyle habits.Additionally, breathing patterns, malocclusion, oral function, and craniofacial morphology were assessed as follows.